Disentangling the roles of RIM and Munc13 in synaptic vesicle localization and neurotransmission
Open accessAbstract
Efficient neurotransmitter release at the presynaptic terminal requires docking of synaptic vesicles to the active zone membrane and formation of fusion-competent synaptic vesicles near voltage-gated Ca2+channels. Rab3-interacting molecule (RIM) is a critical active zone organizer, as it recruits Ca2+channels and activates synaptic vesicle docking and priming via Munc13-1. However, our knowledge about Munc13-independent contributions of RIM to active zone functions is limited. To identify the functions that are solely mediated by RIM, we used genetic manipulations to control RIM and Munc13-1 activity in cultured hippocampal neurons from mice of either sex and compared synaptic ultrastructure and neurotransmission. We found that RIM modulates synaptic vesicle localization in the proximity of the active zone membrane independent of Munc13-1. In another step, both RIM and Munc13 mediate synaptic vesicle docking and priming. In addition, while the activity of both RIM and Munc13-1 is required for Ca2+-evoked release, RIM uniquely controls neurotransmitter release efficiency. However, activity-dependent augmentation of synaptic vesicle pool size relies exclusively on the action of Munc13s. Based on our results, we extend previous findings and propose a refined model in which RIM and Munc13-1 act in overlapping and independent stages of synaptic vesicle localization and release. SIGNIFICANCE STATEMENTThe presynaptic active zone is composed of scaffolding proteins that functionally interact to localize synaptic vesicles to release sites, ensuring neurotransmission. Our current knowledge of the presynaptic active zone function relies on structure-function analysis, which has provided detailed information on the network of interactions and the impact of active zone proteins. Yet, the hierarchical, redundant, or independent cooperation of each active zone protein to synapse functions is not fully understood. Rab3-interacting molecule and Munc13 are the two key functionally interacting active zone proteins. Here, we dissected the distinct actions of Rab3-interacting molecule and Munc13-1 from both ultrastructural and physiological aspects. Our findings provide a more detailed view of how these two presynaptic proteins orchestrate their functions to achieve synaptic transmission.
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The C2A domain of Munc13-1 interacts with the zinc-finger domain of RIM building a heterodimeric complex.
“In contrast, the C2A domain of Munc13-1 interacts with the zinc-finger domain of RIM building a heterodimeric complex [72,89–91].”
From Presynaptic cAMP-PKA-mediated potentiation induces reconfiguration of synaptic vesicle pools and channel-vesicle coupling at hippocampal mossy fiber boutons (2024) · cites this paper as [90]
The Introduction describes RIM–Munc13 interactions, and the References list a study titled “Heterodimerization of Munc13 C2A domain with RIM regulates synaptic vesicle docking and priming.” These passages support the C2A–RIM heterodimer, but our copy does not identify RIM’s zinc-finger domain as the interaction site. (LLM, conf=0.84)
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Exploring the structural dynamics of the vesicle priming machinery
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Stable and Flexible Synaptic Transmission Controlled by the Active Zone Protein Interactions
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Molecular mechanism of synaptic vesicles recycling : role of the Phospholipid Scramblase-1 (PLSCR1)
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- Authors
- Zarebidaki, F., Camacho, M., Brockmann, M. M., Trimbuch, T., Herman, M. A., & Rosenmund, C.
- Affiliations
- NeuroCure Cluster of Excellence (DE)
- Corresponding author
- Rosenmund, Christian
- ORCID
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2020-11-02
- Volume
- 40
- Issue
- 49
- Pages
- 9372-9385
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC7724145
- OpenAlex
- W3097320121
- Cited by
- 37
- References
- 64
- Citations by year
- 2026: 2 · 2025: 3 · 2024: 5 · 2023: 6 · 2022: 15 · 2021: 5 · 2020: 1
- FWCI
- 3.37
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Locations
- Journal of Neuroscience (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Funders
- German Research Council (SFB958, Reinhart Koselleck project)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Extracellular vesicles in disease
- Keywords
- RIM, Munc13-1, Munc13, synaptic vesicle docking, synaptic vesicle priming, active zone, neurotransmitter release, presynaptic terminals, voltage-gated calcium channels, activity-dependent synaptic plasticity, hippocampal neurons, synaptic ultrastructure
- MeSH terms
- Animals, Cells, Cultured, Female, Hippocampus, Male, Mice, Inbred C57BL, Nerve Tissue Proteins, Synaptic Transmission, Synaptic Vesicles, Neurotransmitter Agents, ATP-Binding Cassette Transporters, Glutamic Acid, Mice, Electrophysiological Phenomena
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